Abstract
Many bacteria form spores in response to adverse environmental conditions. Several sporulation pathways have evolved independently and occur through distinctive mechanisms. Here, using cryo-electron tomography (cryo-ET), we examine all stages of growth and exospore formation in the model organism Streptomyces albus. Our data reveal the native ultrastructure of vegetative hyphae, including the likely structures of the polarisome and cytoskeletal filaments. In addition, we observed septal junctions in vegetative septa, predicted to be involved in protein and DNA translocation between neighboring cells. During sporulation, the cell envelope undergoes dramatic remodeling, including the formation of a spore wall and two protective proteinaceous layers. Mature spores reveal the presence of a continuous spore coat and an irregular rodlet sheet. Together, these results provide an unprecedented examination of the ultrastructure in Streptomyces and further our understanding of the structural complexity of exospore formation.
Highlights
Bacterial sporulation encompasses a diverse set of developmental processes which culminate in the production of specialized dormant life forms called spores
Our results were consistent with reports on S. coelicolor sacculi, where the apical region appeared thicker than the lateral wall (Ultee et al, 2020), we did not observe distinct lamellae of cellulose-like polymers and PG at the hyphal tips in S. albus
Our study shows the complete life cycle of Streptomyces from vegetative growth, through sporulation and germination in unprecedented detail revealed by cryo-electron tomography (cryo-ET)
Summary
Bacterial sporulation encompasses a diverse set of developmental processes which culminate in the production of specialized dormant life forms called spores. Spores are morphologically distinct from vegetative cells, often having additional protective structures on the surface such as modified peptidoglycan (PG) and proteinaceous layers. The most extensively characterized mode of sporulation, both genetically and structurally, is endospore formation in Firmicutes, exemplified by Bacillus subtilis (Higgins and Dworkin, 2012; Tocheva et al, 2013; Khanna et al, 2019). Exospore formation, on the other hand, has been extensively characterized in the multicellular bacteria Streptomyces, members of the phylum Actinobacteria. Streptomyces grow vegetatively as a series of interconnected multinucleate compartments, forming multicellular branching filamentous hyphae. Nutrient limitation triggers sporulation and the process begins by the emergence of specialized non-branching aerial hyphae from the colony surface (McCormick and Flardh, 2012; Figure 1). While Streptomyces sporulation is phenotypically similar to many filamentous fungi, these processes are the result of convergent evolution
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